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Higham T.E. (2011) Feeding Mechanics. In: Farrell A.P., (ed.), Encyclopedia of Fish Physiology: From Genome to Environment, volume 1, pp. 597–602. San Diego: Academic Press.

ª 2011 Elsevier Inc. All rights reserved. Author's personal copy

Feeding Mechanics TE Higham, Clemson University, Clemson, SC, USA

ª 2011 Elsevier Inc. All rights reserved.

How Do Fishes Capture Prey? Ecomorphology of Feeding Feeding in Jawless Fishes Jaw Protrusion The Evolution of Suction Feeding The Integration of Locomotion and Feeding What Is Suction-Feeding Performance? Future Directions Hydrodynamics of Suction Feeding Further Reading

Glossary movement. The movements of the particles during Buccal cavity The mouth (oral) cavity at the anterior feeding are captured using high-speed video. end of the fish in front of the gills. Ecomorphology The relationship between morphology Digital particle image velocimetry (DPIV) A modern and ecology. computational technique used to visualize the Exaptation A character, previously shaped by natural movement of fluids. Neutrally buoyant reflective selection for a particular function, that later is co-opted particles are placed in the water, illuminated using a for a new use. laser light sheet and are used to measure water Ram The forward movement of the fish.

How Do Fishes Capture Prey? The prevalence of suction feeding is the major focus of this article. The mechanisms underlying suction feeding Suction (mouth expansion), ram (forward swimming), in fishes are fairly complex. For example, the initial and manipulation are three mechanisms of prey expansive phase is a result of hyoid depression, cranial capture in fishes. Despite the considerable diversity rotation, jaw protrusion, and jaw opening. The muscula­ among the approximately 28 000 species of fishes, ture involved in feeding is discussed in other articles (see the most common mode of prey capture involves also The Muscles: Cartilaginous Fishes Cranial Muscles suction feeding. Although the general principles and Bony Fish Cranial Muscles). underlying suction feeding are relatively straightfor­ ward, several aspects of the feeding system can be modulated in order to alter feeding performance. For Ram example, the rate and magnitude of mouth expansion, the distance between the fish’s mouth and prey item, Several species of fishes capture prey without generating and body movements will influence suction-feeding suction or manipulating the prey. Ram feeding occurs performance. Jaw protrusion is an additional feature when a fish swims over a prey item with its mouth open. that can enhance suction-feeding performance. Based Examples of fishes that employ ram include tunas and on recent evidence, intraoral processing (chewing) also whale sharks. appears to be a relatively common feature among fishes. For example, bowfin (Amia calva), salmonids (e.g., Salmo salar), and pike (e.g., Esox niger)all chew Suction prey with their oral jaws. Modern experimental techniques, including sonomicrometry, digital particle As indicated above, suction feeding is the most common image velocimetry (DPIV), in vivo pressure recordings, mode of prey capture. It involves the rapid expansion of and computational fluid dynamics, all have propelled the buccal cavity, which ultimately draws water into the our understanding of the biomechanics of feeding in mouth due to a pressure gradient formed (Figure 1). The fishes. Some websites include videos that show exam­ majority of bony fishes (Osteichthyes) employs suction ples of these features of fish feeding (see the Relevant feeding in order to capture prey (see Video Clip 1 for an Websites section). example of a fish employing suction feeding).

597 Encyclopedia of Fish Physiology: From Genome to Environment, 2011, Vol. 1, 597-602, DOI: 10.1016/B978-0-1237-4553-8.00216-1 Author's personal copy 598 Buoyancy, Locomotion, and Movement in Fishes | Feeding Mechanics

The Evolution of Suction Feeding

The invasion of new habitats by early fishes was likely facilitated by the evolution of jaws. The diversity of gnathostomes (jawed fishes) exploded in the Silurian and gnathostomes is currently represented by the chondricth­ yans and bony fishes. Later advances, such as jaw protrusion (discussed later) and pharyngeal jaws, then enhanced the basic feeding plan. However, it is important to discuss first the origin of jaws and ultimately suction feeding. Jaws evolved in fishes over 460 million years ago. Recently, two hypotheses have been put forth explaining Figure 1 Suction feeding in the silverspotted sculpin, Blepsias the origin of jaws. Several commonalities persist in both cirrhosus. These images highlight the extent to which the jaw is hypotheses. For example, both agree that jaws represent protruded during suction feeding and the fact that ram the first branchial arch, also termed the mandibular arch (swimming) is not necessary for capturing prey with suction feeding. (Figure 2). The evidence supporting this includes the fact that most of the elements of the jaws (skeletal elements, muscles, etc.) resemble those of other branchial arches. Also, both agree that the lower jaw resides in the ancestral position of the mandibular arch, whereas the upper jaw Manipulation (a) In addition to suction and ram, fishes can obtain prey by physically contacting it and bringing it into the mouth, that is, biting. For example, biting is relatively common among shark and teleost fishes. Every species of hetero­ dontid sharks is ecologically and functionally specialized for durophagy, which involves the consumption of hard prey such as mollusks or crabs. In many cases, the oral jaws of fishes are used to bite a prey item that is located on the substratum. Furthermore, some fishes will bite other animals (e.g., specialized for eating scales) and (b) some will bite off small pieces of plants. As explained below, jawless fishes also use manipulation in order to obtain food.

Feeding in Jawless Fishes

Hagfishes and lampreys feed in a complex and very (c) different way compared with other fishes (see also Hagfishes and Lamprey: Hagfishes, Lampreys: Energetics and Development, and Lampreys: Environmental Physiology). The feeding system includes posteriorly directed keratinous teeth that are attached to dental plates, a paired series of cartilages. The dental plates are moved in and out of the mouth during feeding via retractor and protractor muscles. The movement of the dental plate acts in a similar way to a Figure 2 A hypothetical schematic the evolution of jaws for fixed pulley. This system appears to have both advan­ suction feeding. (a) Here the mandibular (blue) and hyoid (green) tagesanddisadvantagesrelativetofisheswith jaws. The arches before being involved in the jaws. (b) Here the mandibular pulley system allows maximal force transmission, but arch has become the jaws, which are suitable for respiration. In this amphistylic jaw suspension, the mandibular arch is directly does not permit speed amplification. Speed amplifica­ connected tot the cranium. (c) Here the mandibular arch is not tion is likely a key aspect of jaws that has facilitated the directly connected with the cranium, which is more suitable for success of jawed fishes. feeding. Author's personal copy Buoyancy, Locomotion, and Movement in Fishes | Feeding Mechanics 599 stems from the forward extension (in front of the mouth 100 opening) of the maxillary part of the mandibular arch (see also The Skeleton: Bony Fish Skeleton). The first hypothesis for the origins of jaws is the neo­ classical hypothesis, which asserts that the jaw first evolved for stronger ventilation and then to grasp prey. As ventila­ tion increases, prey would be sucked in and potentially consumed. Thus, what originally began with a ventilatory function eventually became utilized for suction feeding, 20 indicating that the current use in feeding is an exaptation. Relative peak fluid speed (%) 0 Eventually, the ability to grasp prey was improved when 0 0.5 1.0 dentition became associated with the mandibular arches. In Distance from mouth aperture the neoclassical hypothesis, few or no oral structures were (maximum mouth diameters) lost during the jawless-to-jawed transition. Figure 3 The general relationship between fluid speed and The second hypothesis for the evolution of the jaws is relative distance from the mouth opening (aperture). Fluid speed the heterotopic hypothesis, which is based mainly on mod­ drops off exponentially going away from the mouth aperture, ern developmental studies. This hypothesis asserts that the highlighting the importance of being close to the prey item for upper jaw did not evolve through a series of intermediate succesful suction feeding. The black circle indicates the location that fluid speed is typically measured using digital particle image stages. Instead, certain genes are expressed farther back in velocimetry (DPIV). the head of gnathostomes compared with lamprey embryos, which leads to different skeletal structures being generated by different parts of the neural crest between the two clades. generated by suction in centrarchid fishes and sharks. The speed of the water being sucked into the fish’s mouth is highest at the mouth aperture and decays What Is Suction-Feeding Performance? rapidly moving away from the fish’s mouth (Figure 3). Thus, suction feeding is most effective when the mouth of In general, generating high fluid speeds (due to negative the predator is in very close proximity to the prey item. pressure in the mouth cavity) during suction feeding is Direct measurements of fluid flow permit the calcula­ a good indication of suction-feeding performance. tion of the ingested volume, which is strongly correlated However, several other factors have been implicated in with mouth size. Because the flow of water is unidirec­ suction-feeding performance, including the ingested tional in fishes (i.e., flows in the mouth and out the volume of water (IVW), the volumetric flow rate, strike opercular cavity), the amount of water ingested can accuracy, and fluid acceleration. The importance of these exceed the size of the buccal cavity. In addition to the metrics depends on the ecology of the fish. For example, size, one can also calculate the shape of the IVW, which is largemouth bass (Micropterus salmoides) depend strongly strongly influenced by swimming speed. on a large IVW and high ram speeds in order to capture Swimming during suction feeding can alter the hydro­ prey. For this species, maximum fluid speed is likely not dynamics of suction feeding. Direct measurements from as important for capturing prey. Thus, species-dependent bluegill sunfish and largemouth bass indicate that, as metrics of suction-feeding performance are necessary to swimming speed increases, the ingested volume becomes understand the feeding diversity of fishes. increasingly narrow and elongate (Figure 4). For further details, see section The Integration of Locomotion and Feeding. Hydrodynamics of Suction Feeding

Modern techniques have greatly enhanced our understand­ Modeling ing of feeding mechanics in fishes. One such area that has contributed substantially is hydrodynamics. Advances have When experimental measurements are difficult (or emerged in both experimental and modeling techniques. impossible) to obtain, modeling the flow of water becomes increasingly informative. In addition, modeling allows one to predict the effects of manipulating a single variable Visualization of Fluid Movement while holding everything else constant. Modeling can The flow of water generated during suction feeding can ultimately provide insight into animal diversity and pre­ be quantified using DPIV, which is a modern computa­ dator–prey interactions. Several attempts have been made tional technique used to visualize the flow of fluids. This to model the hydrodynamics of suction feeding in fishes. technique has recently been utilized to study the flow In the early 1980s, the expanding mouth cavity was Author's personal copy 600 Buoyancy, Locomotion, and Movement in Fishes | Feeding Mechanics

A

B Prey location Strike Length of IVW accuracy Height of IVW

Ingested volume

Figure 4 The influence of swimming (ram) speed on the shape of the ingested volume of water (IVW) and strick accuracy. In situation A, the forward swimming speed of the predator is negligible and prey item A is caught. However, prey B cannot be caught because the IVW is not long enough. In situation B, there is substantial ram speed and prey B is caught. However, prey A cannot be caught because the IVW is too narrow. Ultimately, the length of the IVW, and the location of the prey, will play a large role in capture success. modeled as a single truncated cone with a gape (anterior relationship between diet and structural aspects of the end) and a posterior height. A number of input parameters mouth. Recent work has provided a functional foundation define how the buccal cavity expands. This model yielded for such studies, making the link between morphology pressure and fluid speed for given dimensions and expan­ and ecology more evident. For example, mouth size is sion profile of the feeding event. More than 20 years later, strongly correlated with prey size such that species with the model was modified to include three truncated cones larger mouths are able to ingest larger prey items. connected in series. Jaw lever mechanics are commonly studied in relation Recently, the early model was tested by measuring to ecology. One can measure the closing and opening in- both pressure and fluid speed simultaneously during suc­ and out-levers of the jaw, and then relate that to the diet tion feeding in largemouth bass and bluegill sunfish or feeding style of the predator. In coral reef fishes of the (Lepomis macrochirus). Pressure transducers were Caribbean, species that use their oral jaws to grip, manip­ implanted through the dorsal aspect of the skull and ulate, bite, shred, or crush prey have very high jaw closing they ultimately protruded into the buccal cavity. DPIV lever ratios. In contrast, those species that exhibit ram- or was used to quantify fluid speed. The dimensions of the suction-based strike tactics exhibit much lower jaw clos­ buccal cavity, and the profile of expansion, were also used ing ratios. Higher closing ratios indicate the ability to to predict fluid speed using the early model. Ultimately, more efficiently transmit the force generated by the mus­ the predicted values of fluid speed exceed those measured cles to the tooth surface. Jaw opening ratios do not show under in vivo conditions. Reasons that the model could an obvious pattern like the jaw closing ratios. not fully explain the actual fluid speeds may include The ecomorphology of feeding in cottid fishes (scul­ complex patterns of expansion within the mouth cavity pins) has also been examined in detail. The focus has and/or unsteady flow normal to the long axis of the fish. primarily been on the species of the Northeastern However, more work is needed to understand the Pacific. In these studies, a larger mouth was linked to dynamics of water flow inside the mouth of a fish. feeding on more elusive prey (i.e., fishes, shrimp, mysids, Another technique for modeling fluid flow during and octopods). In addition to the general ecomorphologi­ suction feeding is computational fluid dynamics - a cal approach, functional studies have also been used to branch of fluid dynamics that utilizes the incompressible test whether the morphology exhibited by some species Navier–Stokes equations, which govern the flow of water enhances their performance in an ecological context. during suction feeding. An interesting conclusion from a Larger-mouthed species of sculpins exhibit significantly recent study is that prey size is a very important factor higher capture success on evasive shrimp than did smal­ when considering the timing and magnitude of peak ler-mouthed species. This functional link is critical for forces exerted on prey. Based on modeling, it is apparent providing a mechanism underlying the correlation that peak force can be reached most quickly for prey items between morphology and ecology. that are approximately 33% of mouth diameter. This has important implications for prey selection by fishes. Jaw Protrusion

Ecomorphology of Feeding As mentioned above, the flow of water generated by suction is limited to a narrow range outside of the fish’s The relationships between morphology and ecology, and mouth. Thus, being able to get extremely close to a prey ultimately performance, have been well studied in fishes. item is necessary for effective suction feeding. Jaw pro­ In particular, several studies have focused on the trusion is one way in which the mouth can be extended Author's personal copy Buoyancy, Locomotion, and Movement in Fishes | Feeding Mechanics 601 closer to the prey without having to move the entire body Pectoral Fins (Figure 1). Taken another way, the predator could initi­ As outlined earlier in this article, strike accuracy is neces­ ate a strike at a farther distance from the prey. sary for successful prey capture in fishes, especially those The ability of fishes to protrude their upper jaw has species that rely heavily on suction. In acanthomorph been cited as a key innovation that facilitated the trophic fishes, the pectoral fins are well suited for braking without diversity among fishes. The premaxilla is rotated or inducing any unsteady maneuvers because of their loca­ pushed into an extended position, and multiple paths to tion relative to the fish’s center of mass (see also jaw protrusion have evolved. The upper jaw movement Buoyancy, Locomotion, and Movement in Fishes: can involve anterior, anterodorsal, or anteroventral Paired Fin Swimming). For these fishes, the reaction aspects, and the lower jaw or mandible can pivot around force generated by the pectoral fins during braking goes a ball and socket articulation. through the center of mass, thus maintaining the fish’s Recent work has revealed that jaw protrusion enhances position. Many fishes brake during prey capture, but why forces exerted on a prey item. Although this had been they do this is still in question. One explanation is that suggested for quite some time, empirical data exploring braking reduces the approach speed, which will allow the the functional ramifications of jaw protrusion are limited. predator to adjust its position relative to the prey. Thus, Utilizing a framework based on data from bluegill sunfish, braking may increase capture success. Another possible a recent study utilized empirical data and simulations to benefit to braking during prey capture is that it puts the calculate the contribution of jaw protrusion to the forces predator in a position to quickly maneuver and follow the exerted on prey. The observed speed of jaw protrusion prey if it escapes. Finally, braking might prevent a colli­ was positively correlated with the peak measured force on sion with the substrate (if the prey is located close to the prey. Ultimately, the independent source of accelera­ structure), which will ultimately prevent injury. tion provided by jaw protrusion can increase the total force on the prey by up to 35%.

Future Directions

The Integration of Locomotion Where is the field of feeding mechanics in fishes headed? and Feeding With an increased understanding of the hydrodynamics and mechanics of suction feeding, we are now poised to For several reasons, locomotion is critical for most fishes explore the incredible diversity that is evident in the to successfully capture prey. Locomotor performance many thousands of extant species of fishes. In addition, (e.g., maximum swimming speed and maximum accelera­ few studies have attempted to understand the evolution of tion) will be important for overtaking an evasive or feeding mechanics, in part due to the incomplete under­ elusive prey item. In addition, controlling the locomotor standing of the mechanics and also a lack of well-resolved system (e.g., stability and positioning) will play a signifi­ phylogenies. This will be a fruitful area of research in the cant role in the timing and accuracy of a strike, which will future. Finally, although we know much about the feeding ultimately determine capture success. and locomotor systems, our understanding of how multi­ ple complex systems are integrated is poor. How do fishes move and rapidly expand their mouths with coordinated timing? What underlying neural control mechanisms per­ Ram Speed mit the simultaneous actions of the systems? Although ram is often a component of a feeding event, the relative contribution can vary considerably. One ramifi­ See also: Buoyancy, Locomotion, and Movement in cation of increased ram speed is a decreased capture Fishes: Experimental Hydrodynamics; Maneuverability; success. Among other things, swimming fast during prey Paired Fin Swimming. Hagfishes and Lamprey: capture decreases the time that the predator has to adjust Hagfishes; Lampreys: Energetics and Development; its position relative to the prey. This can result in poor Lampreys: Environmental Physiology. The Muscles: aiming and/or incorrect timing of mouth opening. One Bony Fish Cranial Muscles; Cartilaginous Fishes Cranial critical aspect of suction feeding that is altered with ram Muscles. The Skeleton: Bony Fish Skeleton. speed is the shape of the IVW (Figure 4). As a fish swims faster during feeding, the resulting IVW will be increas­ ingly elongate and narrow. This is important with respect Further Reading to positioning of the prey in front of the predator’s mouth. Carroll AM, Wainwright PC, Huskey SH, Collar DC, and Turingan RG If the prey item is located farther away from the predator, (2004) Morphology predicts suction feeding performance in an elongated IVW will facilitate prey capture. centrarchid fishes. Journal of Experimental Biology 207: 3873–3881. Author's personal copy 602 Buoyancy, Locomotion, and Movement in Fishes | Feeding Mechanics

Day SW, Higham TE, Cheer AY, and Wainwright PC (2005) Spatial and Svanback R, Wainwright PC, and Ferry-Graham LA (2002) Linking temporal patterns of water flow generated by suction feeding bluegill cranial kinematics, buccal pressure, and suction feeding sunfish Lepomis macrochirus resolved by particle image velocimetry. performance in largemouth bass. Physiological and Biochemical Journal of Experimental Biology 208: 2661–2671. Zoology 75(6): 532–543. Higham TE (2007) Feeding, fins and braking maneuvers: Locomotion Van Wassenbergh S and Aerts P (2009) Aquatic suction feeding during prey capture in centrarchid fishes. Journal of Experimental dynamics: Insights from computational modelling. Journal of the Biology 210: 107–117. Royal Society Interface 6: 149–158. Higham TE, Day SW, and Wainwright PC (2005) Sucking while Wainwright PC, Carroll AM, Collar DC, et al. (2007) Suction feeding swimming: Evaluating the effects of ram speed on suction generation mechanics, performance, and diversity in fishes. Integrative and in bluegill sunfish Lepomis macrochirus using digital particle image Comparative Biology 47: 96–106. velocimetry. Journal of Experimental Biology 208: 2653–2660. Wainwright PC, Ferry-Graham LA, Waltzek TB, et al. (2001) Evaluating Higham TE, Day SW, and Wainwright PC (2006) Multidimensional the use of ram and suction during prey capture by cichlid fishes. analysis of suction feeding performance in fishes: Fluid speed, Journal of Experimental Biology 204: 3039–3051. acceleration, strike accuracy and the ingested volume of water. Westneat MW (2004) Evolution of levers and linkages in the feeding Journal of Experimental Biology 209: 2713–2725. mechanisms of fishes. Integrative and Comparative Biology Holzman RA, Day SW, Mehta RS, and Wainwright PC (2008) Jaw 44: 378–389. protrusion enhances forces exerted on prey by suction feeding Wilga CD, Motta PJ, and Sanford CP (2007) Evolution and ecology of fishes. Journal of the Royal Society Interface 5: 1445–1457. feeding in elasmobranchs. Integrative and Comparative Biology Lauder GV (1980) The suction feeding mechanism in sunfishes (Lepomis): 47: 55–69. An experimental analysis. Journal of Experimental Biology 88: 49–72. Mallatt J (2008) The origin of the vertebrate jaw: Neoclassical ideas versus newer, development-based ideas. Zoological Science 25: 990–998. Motta PJ (1984) Mechanics and functions of jaw protrusion in teleost fishes: A review. Copeia 1984: 1–18. Relevant Websites Muller M, Osse JWM, and Verhagen JHG (1982) A quantitative hydrodynamical model of suction feeding in fish. Journal of http://www.youtube.com/watch?v¼AWsbwQ­ Theoretical Biology 95: 49–79. yxw4&feature¼related – You Tube; Freshwater eel, Anguilla Nemeth DH (1997) Modulation of buccal pressure during prey capture in sp., feeding. Hexagrammos decagrammus (Teleostei: Hexagrammidae). Journal http://www.youtube.com/watch?v¼MSzEGg-6wWo – You of Experimental Biology 200: 2145–2154. Norton SF (1995) A functional approach to ecomorphological patterns of Tube; Particle image velocimetry video of suction feeding by feeding in cottid fishes. Environmental Biology of Fishes 44: 61–78. a bluegill sunfish, Lepomis macrochi. Norton SF and Brainerd EL (1993) Convergence in the feeding mechanics http://www.youtube.com/watch?v¼OHivHHmYSDc – You of ecomorphologically similar species in the Centrarchidae and Tube; Particle image velocimetry video of suction feeding by Cichlidae. Journal of Experimental Biology 176: 11–29. Sanford CPJ and Wainwright PC (2002) Use of sonomicrometry a largemouth bass, Micropterus salmoides. demonstrates the link between prey capture kinematics and suction pressure in largemouth bass. Journal of Experimental Biology For supplementary material please also visit the companion site: 205: 3445–3457. http://www.elsevierdirect.com/companions/9780123745453